other waterways, severely impairing invertebrate assemblages as well as causing
sublethal and sometimes lethal toxicity to fishes [1, 28, 39, 40]. Newer pyrethroids
(e.g., cypermethrin) are generally more toxic than older formulations, especially to
aquatic invertebrates that are physiologically most similar to the insects which these
chemicals are designed to target [6, 26, 41–43]. Cypermethrin, for example,
hydrolyzes more slowly than Type I pyrethroids such as permethrin, resulting in a
toxic potency up to 20-fold greater [41]. In fact, pyrethroids have often been
implicated in causing sediment toxicity to the amphipod Hyalella azteca commonly
used for bioassessments in urban and/or agricultural areas [44–48]. And while
pyrethroids used in agriculture still contribute to aquatic impairment, urban pyrethroid inputs have been cited as a major source of pyrethroid contamination in the
environment. Bifenthrin, cyfluthrin, and cypermethrin cause the most concern in
waterways surrounded by residential and urban areas [49, 50]. Bifenthrin applied by
homeowners and structural pest control professionals has reached levels in the water
column during storm events that are sufficient to cause acute invertebrate toxicity
[25, 42]. In fact, for the period 2009–2015, bifenthrin has shown one of the highest
risk quotients in inland surface waters in the European Union [51].
For these numerous reasons, pyrethroids are ubiquitous in the aquatic environment. They have long been implicated as a strong selective pressure in the pest
species they are meant to control [52–55], and accumulating evidence now shows
they are capable of driving resistance in nontarget aquatic organisms exposed to
pyrethroids unintentionally [56–63]. In the present work, we briefly review the acute
and sublethal effects of pyrethroid exposure for invertebrates and insects in aquatic
ecosystems. We then focus on the evidence of increased tolerance to pyrethroids that
has been documented in pests that inhabit pyrethroid-laden aquatic environments
such as sea lice, as well as nontarget life stages of mosquitoes and black flies, and
nontarget aquatic invertebrates (cladocerans, amphipods), with an emphasis on
adaptive resistance (Fig. 1). In doing so, we describe the influence of pyrethroid
use in the environment in the context of evolutionary toxicology. Finally, we explore
the ecological and evolutionary implications of pyrethroids as a strong selective
pressure driving resistance in the aquatic environment and discuss impacts on
evolutionary processes, ecosystems, and risk assessment.
2 Acute Toxicity
A wealth of literature exists concerning the acute toxicity of pyrethroids to aquatic
organisms, and this topic is extensively reviewed elsewhere [6, 19, 64–67]. Acute
mortality has been documented far below the 1 μg L
À1 range for fish, crustaceans,
and insects [6] with the amphipod H. azteca being among the most sensitive (Fig. 2),
having a 96 h LC 50 (median lethal concentration) in the low ng L
À1 range [6, 57, 58,
68]. Acute toxicity has even been documented at levels below 1 ng L
À1 [43]. A
review by Mian and Milla [66] illustrated that that many nontarget aquatic insects
(Ephemeroptera, Odonata, Plecoptera, Hemiptera, Coleoptera, Trichoptera) and
The Ecological and Evolutionary Implications of Pyrethroid Exposure: A New. . .
113
sublethal and sometimes lethal toxicity to fishes [1, 28, 39, 40]. Newer pyrethroids
(e.g., cypermethrin) are generally more toxic than older formulations, especially to
aquatic invertebrates that are physiologically most similar to the insects which these
chemicals are designed to target [6, 26, 41–43]. Cypermethrin, for example,
hydrolyzes more slowly than Type I pyrethroids such as permethrin, resulting in a
toxic potency up to 20-fold greater [41]. In fact, pyrethroids have often been
implicated in causing sediment toxicity to the amphipod Hyalella azteca commonly
used for bioassessments in urban and/or agricultural areas [44–48]. And while
pyrethroids used in agriculture still contribute to aquatic impairment, urban pyrethroid inputs have been cited as a major source of pyrethroid contamination in the
environment. Bifenthrin, cyfluthrin, and cypermethrin cause the most concern in
waterways surrounded by residential and urban areas [49, 50]. Bifenthrin applied by
homeowners and structural pest control professionals has reached levels in the water
column during storm events that are sufficient to cause acute invertebrate toxicity
[25, 42]. In fact, for the period 2009–2015, bifenthrin has shown one of the highest
risk quotients in inland surface waters in the European Union [51].
For these numerous reasons, pyrethroids are ubiquitous in the aquatic environment. They have long been implicated as a strong selective pressure in the pest
species they are meant to control [52–55], and accumulating evidence now shows
they are capable of driving resistance in nontarget aquatic organisms exposed to
pyrethroids unintentionally [56–63]. In the present work, we briefly review the acute
and sublethal effects of pyrethroid exposure for invertebrates and insects in aquatic
ecosystems. We then focus on the evidence of increased tolerance to pyrethroids that
has been documented in pests that inhabit pyrethroid-laden aquatic environments
such as sea lice, as well as nontarget life stages of mosquitoes and black flies, and
nontarget aquatic invertebrates (cladocerans, amphipods), with an emphasis on
adaptive resistance (Fig. 1). In doing so, we describe the influence of pyrethroid
use in the environment in the context of evolutionary toxicology. Finally, we explore
the ecological and evolutionary implications of pyrethroids as a strong selective
pressure driving resistance in the aquatic environment and discuss impacts on
evolutionary processes, ecosystems, and risk assessment.
2 Acute Toxicity
A wealth of literature exists concerning the acute toxicity of pyrethroids to aquatic
organisms, and this topic is extensively reviewed elsewhere [6, 19, 64–67]. Acute
mortality has been documented far below the 1 μg L
À1 range for fish, crustaceans,
and insects [6] with the amphipod H. azteca being among the most sensitive (Fig. 2),
having a 96 h LC 50 (median lethal concentration) in the low ng L
À1 range [6, 57, 58,
68]. Acute toxicity has even been documented at levels below 1 ng L
À1 [43]. A
review by Mian and Milla [66] illustrated that that many nontarget aquatic insects
(Ephemeroptera, Odonata, Plecoptera, Hemiptera, Coleoptera, Trichoptera) and
The Ecological and Evolutionary Implications of Pyrethroid Exposure: A New. . .
113